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Polish suture zone as the goblet of truth in post-glacial history of mammals in Europe

  • Joanna StojakEmail author
  • Ewa Tarnowska
Open Access
Review Article
  • 206 Downloads

Abstract

Present-day species distribution and patterns of genetic diversity in Europe are a result of post-glacial re-colonization from glacial refugia after the Last Glacial Maximum. This process led to the formation of secondary contact zones (suture zones) between the haplogroups of different species, and were induced by several factors, including climate and evolutionary processes like selection and adaptation. One such suture zone has been found in Poland, where a complex network of different phylogenetic lineages of predators, ungulates, and rodents is present. The phylogeography of mammals in western Europe has been widely studied, but central and eastern Europe have been treated cursorily. Only a few samples from these areas were analyzed in previous studies, resulting in a simplified and false description of local genetic structure. In this review, results of previous phylogeographic studies on carnivore, ungulate, and rodent species from central and eastern Europe were collected and synthesized to verify the Polish suture zone hypothesis and examine how it is affected by different variables (geomorphological features like the Carpathian Mountains and Vistula River, climate, or anthropogenic factors). Our data reflects the importance of precise studies in this region and the value they contribute to further studies of large-scale European phylogeography.

Keywords

Contact zone Genetic diversity Last Glacial Maximum Phylogeography Glacial refugia Climatic factors 

Introduction

During the last glaciation (Weichselian; 115 ± 11.5 thousand years ago, kya) (Rasmussen et al. 2014), the Scandinavian ice sheet advanced and retreated multiple times, and different fauna and flora species survived unfavorable conditions in glacial refugia (Hewitt 1999; Avise 2000, 2004; Stewart and Lister 2001; Sommer and Nadachowski 2006). The coldest conditions and maximum extent of the Scandinavian ice sheet were present during the Last Glacial Maximum (LGM; 27.5 to 19 kya; Clark et al. 2009; Hughes et al. 2013; Alvarado et al. 2011), when ice sheets covered the entirety of Scandinavia as well as huge areas in the British Isles, Germany, Poland, and northern parts of the East European Plain (northern Russia). Meanwhile, periglacial areas were covered by an Arctic tundra (Lozinski 1909; Tarasov et al. 2001; Cheddadi and Bar-Hen 2008; Strandberg et al. 2011).

Present-day species distribution in Europe is a result of rapid climate warming after the LGM that induced abrupt post-glacial re-colonization from glacial refugia (Hewitt 1999; Stewart and Lister 2001; Sommer and Nadachowski 2006; Pazonyi 2004; Stewart et al. 2010; Tzedakis et al. 2013; Baca et al. 2017; Quinzin et al. 2017). Since various genetic changes have been retained in organisms that survived in glacial refugia, separate phylogenetic lineages (haplogroups), that reveal the evolutionary history of a species, can be identified (Hewitt 1999; Taberlet et al. 1998; Avise 2000, 2004; Michaux et al. 2003). Therefore, the phylogeography of different mammalian, reptilian, avian, and plant species unravels the post-glacial history of the whole continent (e.g., Davison et al. 2001; Tarasov et al. 2001; Palmé et al. 2003; Kvist et al. 2004; Colangelo et al. 2010; Dool et al. 2013; Montgomery et al. 2014; Herrera 2017; Wielstra et al. 2017; Horreo et al. 2018). Previous studies have shown that species range is determined by multiple factors, such as topographic barriers (e.g., mountain chains, seas, large rivers; Cox and Moore 1993; Tougard et al. 2013; Herrera 2017; Murphy et al. 2017) or specific adaptations to climatic, environmental, and biotic conditions (e.g., competition, predation, food availability; Warren et al. 2000; Dingerkus and Montgomery 2001).

Over the last few decades, numerous phylogeographic studies concerning mammalian species have been conducted in western Europe using different molecular markers—short tandem repeats (STR, microsatellite DNA; e.g., Neumann et al. 2005; Beysard and Heckel 2014; Herman et al. 2019), single nucleotide polymorphisms (SNP; e.g., Kotlík et al. 2018), the Y chromosome (e.g., Herman et al. 2019; Jones and Searle 2015), and different fragments of mitochondrial DNA (mtDNA), such as the control region (D-loop) or cytochrome b gene (e.g., Haynes et al. 2003; Deffontaine et al. 2005; Heckel et al. 2005; Neumann et al. 2005; Saarma et al. 2007; Braaker and Heckel 2009; Searle et al. 2009; Skog et al. 2009; Lebarbenchon et al. 2010; Edwards et al. 2012; Herman et al. 2014; Martínkovà et al. 2013; Kinoshita et al. 2017; Herman et al. 2019). However, only results from studies using maternally inherited mtDNA are accessible (for instance, in GenBank database) and useful for continental comparison. Therefore, we recognize this marker as the most fundamental and commonly used tool in large-scale phylogeography.

In Europe, phylogeography and phylogenetic patterns have contributed to the identification of contact zones between the haplogroups of one species, and even between multiple genetic lineages of different species. This complex co-occurrence of contact zones is known as a “suture zone,” and is maintained by many factors, including climate, selection, and adaptation (Hewitt 1999; Remington 1968). In western Europe, six suture zones have been identified and well-described (Hewitt 1999; Schmitt 2007). Although Remington (1968) suggested that other suture zones could be found in the Ural and central Europe, for a long time, these regions have been treated cursorily and omitted in phylogeographic studies. Moreover, high inaccessibility of data from eastern Europe (such as from the Russian Federation, Belarus, or Ukraine) is also a challenge, as data is frequently published only in Russian, or translated into English with a delay (Pavlov 1999; Abramson et al. 2009; Bulatova et al. 2010; Zhigileva and Gorbacheva 2017; Sibiryakov et al. 2018).

In multiple previous phylogeographic studies, only a few samples from central or eastern Europe have been analyzed, which has resulted in a simplified and incorrect description of genetic structure in this area (e.g., Randi et al. 2004; Deffontaine et al. 2005; Heckel et al. 2005; Neumann et al. 2005; Skog et al. 2009; Meiri et al. 2013). For instance, based on four samples of the common vole (Microtus arvalis) from one location in north-eastern Poland, Haynes et al. (2003) hypothesized that only one phylogenetic lineage is present in central Europe. However, further studies have revealed a more complex pattern of genetic diversity within this species in this area (Stojak et al. 2015, 2016a). Similar findings were detected in the cases of other mammalian species in central Europe. As a result, Wójcik et al. (2010) suggested the presence of a suture zone between species, races, and genetic lineages in Poland, which was consistent with Remington’s (1968) predictions.

In Poland, a strong East-West precipitation gradient, resulting from the collision of wet Atlantic air in the West and dry continental air in the East is present (Starkel 1991; Hijmans et al. 2005; Stojak et al. 2019). During the LGM, Poland was covered by ice in the North and tundra in the South (Wysota et al. 2002, 2009; Marks et al. 2016), in close proximity to the Carpathian Basin—a well-known temperate refugial area (Sommer and Nadachowski 2006; Pazonyi 2004; Tzedakis et al. 2013). Moreover, because it is located in the center of Europe, Poland could be part of natural migration corridor for many fauna and flora species, even from Asia (Trojan 1997).

The main aim of this article was to collect and combine results of previous phylogeographic studies on different mammal species from central and eastern Europe and verify the existence of a suture zone in Poland or central Europe (Wójcik et al. 2010). Such a summary will contribute a comprehensive description of post-glacial re-colonization scenarios of Polish territory by different species of carnivores, ungulates, and rodents. Furthermore, this review also examines the influence of different variables (geomorphological features like the Carpathian Mountains and Vistula River, climate, or anthropogenic factors) on contemporary genetic diversity of mammalian communities and the maintenance of a suture zone in Poland. Ultimately, we assume that the aforementioned combined data from central and eastern Europe highlights the importance of this region in precise studies of large-scale European phylogeography.

Characteristics of a suture zone in Poland

The Polish suture zone is a very wide and complex formation, consisting of multiple contact zones between different haplogroups of at least 11 species of large carnivores, ungulates, and small mammals (Fig.1, Table 1).
Fig. 1

The suture zone in Poland (central Europe) consists of multiple contact zones between different haplogroups of (a) carnivores: –Eurasian lynx (Ll) and gray wolf (Cl); (b) ungulates –roe deer (Cc), red deer (Ce), and European moose (Aa); (c) small predators–weasel (Mn) and pine marten (Mm); and (d) rodents–common hamster (Ccri), bank vole (Cg), common vole (Ma), and field vole (Mag). The Vistula River (blue solid line), as well as the Sudetes and Carpathian Mountains (gray area) are marked on the map of Poland

Table 1

Characteristics of patterns observed for different carnivores, ungulates, and small mammals in the Polish suture zone, including number of lineages/groups (n) identified using different mitochondrial markers, estimated age (in thousand years, kya with a 95% confidence interval) and refugial origin of each lineage/group (BP Balkan Peninsula, IP Iberian Peninsula, AP Apennine Peninsula, CR Carpathian refugium), and factors maintaining contact zones between lineages/groups (CM Carpathian Mountains, VR Vistula river, CE climate and environmental factors, HI human impact)

Species

Mitochondrial marker

n

Lineages/groups

Estimated age (kya)

Refugia location

Factors maintaining contact zones

Reference

Eurasian lynx

(Lynx lynx)

Control region

3

Carpathian

BPF

KARPF

After Last Glacial Maximum (< 19)

CR

CE, HI

Ratkiewicz et al. 2012, 2014

Gray wolf

(Canis lupus)

Control region

2

Haplogroup 1

Haplogroup 2

301 (169–490)

316 (160–493)

AP

IP

HI

Pilot et al. 2010, Czarnomska et al. 2014

European roe deer* (Capreolus capreolus)

Control region, Cytochrome b

3

Central

West

East

190 (150–450)

290 (140–550)

190 (150–450)

IP

IP

BP

CE

Matosiuk et al. 2014a, Olano-Marin et al. 2014

Red deer

(Cervus elaphus)

Control region

2

Haplogroup A

Haplogroup C

A/C

162 (113.6–213)

IP

BP

HI

Skog et al. 2009, Niedziałkowska et al. 2011

European moose

(Alces alces)

Control region

3

Eastern

Western

Central

Eastern/Western/Central

20–35

East European Plain

France/Belgium

CR/BP

HI

Niedziałkowska et al. 2014

Common hamster (Cricetus cricetus)

control region

2

E1

Pannonia

66–115

85–147

East European Plain

CR

CM

Banaszek et al. 2012

Bank vole (Clethrionomys glareolus)

cytochrome b

3

Carpathian

Eastern

Western

40–176

15–160

Unknown

CR

East European Plain

Austria/Western Balkans

CE

Deffontaine et al. 2005, Wójcik et al. 2010, Tarnowska et al. 2016

Weasel (Mustela nivalis)

Cytochrome b

4

Western

Eastern

Balkan

Carpathian

24.8 (13.7–41)

52.8 (27.3–86.9)

35.0 (17.4–56.7)

31.5 (17.2–50.1)

IP/Pyrenees

unknown

BP

CR

CE

McDevitt et al. 2012

Pine marten (Martes martes)

Cytochrome b, tRNAPro, tRNAThr, control region, 12S rRNA

2

Central-Northern Europe

Mediterranean

92 (30–150)

81 (30–140)

CR

Mediterranean Peninsulas

CE

Ruiz-González et al. 2013

Common vole (Microtus arvalis)

Cytochrome b

2

Eastern

Central

22.4 (13.5–29.8)

16.3 (8.5–22.6)

CR

Central Europe

VR, CE

Stojak et al. 2016a

field vole (Microtus agrestis)

Cytochrome b

2

Western

Central Europe

12.4 (8.9–17.2)

Unknown

VR, CE

Jaarola and Searle 2002

Herman and Searle 2011

*Divergence time of C. capreolus and C. pygargus: 810 (350–1210; Matosiuk et al. 2014a)

Apex predators

Two apex predators should be taken into consideration when describing the post-glacial re-colonization of Poland: the Eurasian lynx (Lynx lynx) and the gray wolf (Canis lupus).

There are three groups of lynx present in Poland, although high levels of habitat fragmentation prevent their secondary contact (Fig. 1a, Table 1). The Carpathian population is distinct from the north-eastern one, which is differentiated in two groups (Ratkiewicz et al. 2012, 2014). The BPF group, found only in Białowieża Primeval Forest, is characterized by low genetic variability. On the other hand, the neighboring KARPF group encompasses lynx found in Lithuania, Latvia, Estonia, Finland, and Russia (Ratkiewicz et al. 2014). Observed patterns of genetic diversity suggest that lynx expanded from the Carpathian refugium following the LGM, while the formation of the two northern groups can be attributed to post-glacial re-colonization processes (Ratkiewicz et al. 2014).

In the case of the gray wolf, Pilot et al. (2010) identified a wide contact zone between two haplogroups of this species in southern Poland (Fig. 1a, Table 1). Haplogroup 1, which likely originated from the Apennine Peninsula, was found in Carpathian populations (Pilot et al. 2010). In Poland, haplogroup 2, fixed in the Iberian Peninsula, differentiated into three subpopulations: one found only in south-eastern Poland, a second (and the most abundant) found mainly in western and northern Poland, and a third found in north-eastern Poland (Czarnomska et al. 2013).

Ungulates

Three large herbivorous species (European roe deer Capreolus capreolus, red deer Cervus elaphus, and European moose Alces alces) can be found in the Polish suture zone.

Three mtDNA lineages of European roe deer meet in south-eastern Poland and are referred to as the Central, West, and East clades (Fig. 1b, Table 1; Matosiuk et al. 2014a; Olano-Marin et al. 2014). The Central and West haplogroups probably originated from the Iberian refugium, while the East clade survived the last glaciation on the Balkan Peninsula (Randi et al. 2004). Moreover, Matosiuk et al. (2014a, b) described a very wide contact zone between European and Siberian roe deer (C. pygargus) in the eastern part of Poland.

A similar phylogeographic pattern was found in red deer, a species that survived the last glaciation in western refugia located on the Iberian Peninsula and eastern refugia in the Balkans (Fig. 1b, Table 1; Skog et al. 2009). Two haplogroups (A and C), reflecting the aforementioned evolutionary history of C. elaphus, have been found in Poland, with a contact zone in the central part of the country (Niedziałkowska et al. 2011). Fossil records indicate that red deer were also present in the Carpathian Basin during the Last Glacial Maximum (Sommer and Nadachowski 2006).

In the case of European moose, a contact zone between three haplogroups was identified in central Poland (Fig. 1b, Table 1). The Eastern clade likely re-colonized Europe from refugia located in the Ukraine or Russian Plains, while the Western lineage is thought to have originated from France or Belgium. The Central haplogroup, on the other hand, is believed to have survived the last glaciation in the Carpathian or Balkan refugia (Niedziałkowska et al. 2014).

Small mammals

Polish communities of small mammals probably arose towards the end of the Pleistocene (Nadachowski 1989). Their evolutionary history and routes of post-glacial colonization have been reconstructed on the basis of fossil records, which are important indicators of glacial refugia. Nonetheless, well-preserved skeletons of small mammals were found only in a few locations in southern Poland (Nadachowski 1990; Nadachowski et al. 2009), so genetic markers have instead been used to provide new insight into post-glacial history at a larger scale. Until now, multiple studies on the phylogeography of small mammals, primarily rodents, have been conducted in Poland.

One of these rodents, the common hamster (Cricetus cricetus) is considered a critically endangered species. Genetic studies on small Polish populations have revealed a contact zone between two haplogroups of this species in the Małopolska Upland (southern Poland; Fig. 1d, Table 1; Banaszek et al. 2012). Of these, the Pannonian lineage probably originated from the Carpathian refugium, while the E1 lineage originated from the Russian Plains or Ukrainian steppe (Banaszek et al. 2012).

Another rodent that survived the LGM in the Carpathian refugium is a woodland species, the bank vole (Clethrionomys glareolus; Kotlík et al. 2006). In Poland, three mtDNA lineages have been described and named according to their refugial origin: the Carpathian, Western, and Eastern (Fig. 1d, Table 1; Wójcik et al. 2010). The contact zone between the Carpathian and Eastern lineages is very wide and spread across Poland, from the north-eastern to the south-western part of the country (Wójcik et al. 2010; Tarnowska et al. 2016, 2018). Individuals from the Western clade were found in only a few regions in southern and central Poland (Wójcik et al. 2010; Tarnowska et al. 2016).

A small predator, the weasel (Mustela nivalis), has four haplogroups in Poland (McDevitt et al. 2012). A contact zone between the Carpathian, Western, and Eastern lineages is located in the central part of the country (Fig. 1c, Table 1; McDevitt et al. 2012). In central and southern Poland, a few individuals belonging to the Balkan clade have also been identified (McDevitt et al. 2012).

The European pine marten (Martes martes) presents another example of a small predator’s contact zone. Ruiz-González et al. (2013) discovered two phylogenetic lineages of this species in north-eastern Poland: the central-northern European and Mediterranean lineages (Fig. 1c, Table 1).

Phylogeographic patterns have also been studied for two sibling species, the common vole (Microtus arvalis) and the field vole (Microtus agrestis). These two rodent species are morphologically very similar, but they differ in habitat preferences. The common vole survived the last glaciation in both southern and northern refugia. A contact zone between two haplogroups of this species is located in north-western Poland: the Eastern lineage probably originated in the Carpathian refugium and the Central lineage is thought to have originated in the Alps (Fig. 1d, Table 1; Stojak et al. 2015, 2016a). The field vole, on the other hand, re-colonized central Europe from exclusively southern refugia (Jaarola and Searle 2002; Herman and Searle 2011). In south-western Poland, two mtDNA lineages of this rodent have been found and referred to as the Western and Central-European clades (Fig. 1d, Table 1; Herman et al. 2014).

Factors maintaining the Polish suture zone

The maintenance of a suture zone is a dynamic and multilateral process. In this article, we assume that Polish suture zone formation is the result of post-glacial re-colonization processes from glacial refugia and subsequent adaptations to environmental and climatic conditions. Therefore, in this chapter, we analyze the possible influence of the Carpathians, large river corridors, climate, and human impact on the emergence and maintenance of the Polish suture zone. To fulfill our objective, we compiled and synthesized evidence from the aforementioned phylogeographic studies on various mammalian species found in central Europe.

Carpathian Mountains

The Carpathian Mountains are the largest mountain range in central Europe. During the last glaciation, only high mountain peaks in the Tatra Mountains were covered with ice and snow (Zasadni and Kłapyta 2014), their surroundings were covered by an Arctic tundra (Pazonyi 2004; Sommer and Nadachowski 2006). Fossil records and genetic studies have confirmed the location of a glacial refugium in the Pannonian Basin (Pazonyi 2004), as well as the presence of diversified mammal communities on the northern slopes of the Carpathian Mountains (such as in the Orawa-Nowy Targ Basin, at Obłazowa cave and Obłazowa 2 paleontological sites), during and just after the LGM (Valde-Nowak et al. 2003; Nadachowski et al. 1993; Nadachowski and Valde-Nowak 2015). Records of areas that were once rich in small mammals date back to approximately 25–15 calibrated kya and support the presence of a diverse fauna even within the Tatra Mountains (Horáček et al. 2015).

During the LGM, many different mammals were present in the Carpathian refugium, including red foxes (Vulpes vulpes), brown bears (Ursus arctos), red and roe deer, moose, European pine marten, hedgehogs (Erinaceus sp.), and bank voles (Stewart and Lister 2001; Pazonyi 2004; Kotlík et al. 2006; Sommer and Nadachowski 2006). The geographic location and size of the Carpathian Mountains made this area a well-preserved environment and biodiversity hot spot for many organisms, not only mammals.

Ratkiewicz et al. (2014) showed that the entire contemporary lynx population in central Europe and Scandinavia originated from the Carpathians. According to genetic studies, lynx belonging to BFP and KARPF populations separated from the Carpathian group, and subsequent separations from the BFP and KARPF groups resulted in the formation of separate lynx populations in Russia and Finland, and eventually in Norway.

High mobility of large predators and ungulates allows them to cross mountain ranges or use them as suitable habitats. Nonetheless, the likelihood of mountains acting as a barrier to gene flow varies across species. Pilot et al. (2006) detected no physical barriers to dispersal for wolves in central and eastern Europe, while Niedziałkowska et al. (2016) suggested that high mountain ranges could be a barrier to gene flow in moose populations.

In the case of small mammals, the Carpathians could be a significant geographic barrier, both for migration and gene flow. The Pannonian lineage of the common hamster, which survived the LGM in the Carpathian refugium, re-colonized Poland only through the Moravian Gate, a natural depression between the Carpathian Mountains in the East and the Sudetes in the West (Banaszek et al. 2012). On the other hand, the Balkan lineage of the weasel probably reached Poland through the Carpathian mountain range, though details of this re-colonization are still unknown (McDevitt et al. 2012).

Ultimately, the Carpathian Mountains have significantly influenced—both positively and negatively—the contemporary structure of the Polish suture zone, having acted as both a refugial area for many temperate species and a barrier preventing certain lineages from reaching Polish territory (Table 1).

Vistula river

The Vistula is both the longest and largest river in Poland and one of the longest rivers in Europe. The last glaciation, lasting until 11.7 thousand years ago (kya), was named the Weichselian (Vistulian) glaciation, after this river. During the LGM, the Scandinavian ice sheet covered large areas from the Pskov region in Russia to Denmark, reaching through central Poland (Wysota et al. 2002, 2009; Stroeven et al. 2016). As a result, the Vistula corridor was very broad and covered by permafrost patches (Starkel 1991, 2001; Stojak et al. 2016a). After the Younger Dryas (approximately 11 kya), when the climate rapidly warmed, the ice sheet and permafrost patches on the river melted intensively, causing flooding over a large area. The middle Vistula valley eventually consisted of sand dunes with strong winds that re-shaped it continuously (Starkel 1991, 2001). All of these processes led to the Vistula river acting as a geographic barrier to gene flow for populations of small mammals (Stojak et al. 2016ab). The dynamic processes lasted until 8–9 thousand years ago, when the Vistula corridor consequently started to stabilize (Starkel 1991).

Niedziałkowska et al. (2016) suggested that large areas of water, such as wide river corridors, could be a barrier to migration and gene flow even for swimmers as good as moose. Matosiuk et al. (2014a) revealed that the location of the Vistula river could have had a significant effect on the maintenance of Siberian roe deer mtDNA in the European roe deer genome.

Nevertheless, contemporary genetic structure of small mammal communities in Poland showed no strong evidence that the Vistula could be an important barrier to gene flow. Studies on the contact zone between two haplogroups of the bank vole in north-eastern Poland reported unlimited exchange of genetic information (both mitochondrial and nuclear) between populations located on opposite banks of the river (Tarnowska et al. 2016, 2018). On the other hand, the genetic structures of the common and field voles suggested that the major Polish river delayed gene flow between populations, and that this eventual exchange occurred only in the valley of the lower Vistula (northern Poland; Stojak et al. 2016b, 2019).

Despite their size and physical limitations, small mammals are able to cross long distances and potential geographic barriers with the—usually unintentional—help of humans. Martínková et al. (2013) showed that approximately 5000 years ago, several individuals of the common vole from Belgium were transported by the Neolithic people to the Orkney archipelago, situated off the north coast of Great Britain. Therefore, further studies are needed to more precisely describe the influence and role of the Vistula river in Polish suture zone formation and maintenance (Table 1).

Climate and environmental conditions

The western part of Poland is characterized by a warmer and more humid climate than is found in the eastern part of the country. This has led to contact between different genetic groups that are adapted to variable climatic and environmental conditions.

Ratkiewicz et al. (2014) suggested that latitude and depth of snow cover could have a significant effect on the observed genetic structure of lynx populations. The complex distributions of the Siberian and European roe deer in Poland (including the contact zone between three haplogroups of C. capreolus) are significantly influenced by the number of days that exhibit snow cover, subsequent snow depth, average temperature during the month of January, and the number of days that temperatures fall below freezing throughout the whole year (Matosiuk et al. 2014a).

Pilot et al. (2006) suggested that the genetic differentiation observed among populations of wolves in central Europe could be a result of climate, habitat availability, and habitat conditions influencing the carnivore’s diet. Gula (2004) noticed that snow cover had an effect on predation by wolves, and concluded that predator-prey interactions play an important role in the formation of contemporary patterns in mammal species distribution across Europe.

An even stronger influence of climate was recorded in small mammal populations. Tarnowska et al. (2016) revealed that the occurrence of the Carpathian lineage of bank voles in north-eastern Poland was positively correlated with mean temperature in July and the distribution of plant species associated with the Carpathian refugium. In the case of two sibling species, the common and field voles, average minimum temperature in January most influenced the genetic structure of these rodents in Poland. Additionally, average annual precipitation was also an important factor for the field vole, a species that prefers wet and humid environments (Stojak et al. 2019). These results are in agreement with adaptations observed in Polish populations of weasel, a predator of the voles. According to the description of McDevitt et al. (2012), the distribution of M. nivalis haplogroups significantly depended on the number of days with snow cover throughout the year, as well as the average minimum temperature in January. In general, the Carpathian lineage of weasels was reported to be more adapted to a cold, severe climate than the Balkan lineage.

Climate, environmental conditions, and availability of preferred habitats are crucial factors influencing the distribution of species, lineages, and genetic groups. We predict that lineages fixed in the Carpathian refugium could be more resistant to cold climate than lineages that originated in southern refugia; therefore, climate is likely the leading factor involved in the shaping and maintenance of suture zones in Europe (Table 1).

Human impact

Human activity has a great impact on the biodiversity and genetic structure of species, lineages, and populations worldwide. Excessive hunting and the fragmentation of natural habitats have resulted in the extirpation or endangerment of many species, including the Eurasian lynx and gray wolf (Huck et al. 2010). The Eurasian lynx was once cosmopolitan across Europe, but in the nineteenth century, it was extirpated in the western and central parts of the continent. Nowadays, in central Europe, the species inhabits only the Carpathian Mountains and edges of north-eastern Poland (Ratkiewicz et al. 2012, 2014), as populations are threatened by habitat loss, poaching, and diminution of prey (Schmidt 2008; Schmidt et al. 2011). A similar situation has been observed in the gray wolf (Jędrzejewska et al. 1996; Gula 2008). Ungulate populations, on the other hand, have experienced profound growth following a decrease in the number of apex predators (Jędrzejewski et al. 2012).

During the early twentieth century, all ungulate species described in this article underwent population number declines and changes in their distribution in Poland, mainly due to deforestation and overhunting. Therefore, the contemporary genetic structure of roe deer, red deer and moose is largely the result of introductions and translocations of individuals between populations (Skog et al. 2009; Matosiuk et al. 2014a, b; Świsłocka et al. 2013). Present-day forest management and low pressure from predators, however, have facilitated rather abrupt and unusual range expansions for each of these ungulate species (Jędrzejewski et al. 2012; Matosiuk et al. 2014a).

The contact zone between European and Siberian roe deer in eastern Poland is a result of the introduction of C. pygargus to two locations: the Białowieża Primeval Forest in 1891 (Pavlov 1999) and Silesia in 1909 (Gleiss 1967). In the case of red deer, while the distribution of the Eastern haplogroup is a result of post-glacial re-colonization, the pattern observed for the western clade seems to be artificial and shaped by the reintroduction of this species to areas where it was previously extirpated (Niedziałkowska et al. 2011, 2012). Likewise, after the Second World War, moose came close to extinction, and only a few isolated populations from north-eastern Poland, East Prussia, and Sweden survived throughout central Europe (Gębczyńska and Raczyński 2004; Schmölcke and Zachos 2005; Charlier et al. 2008; Steinbach 2009; Świsłocka et al. 2013). In Poland, the relict population, found in the Biebrza marshes, is characterized by the presence of a unique H1 haplotype (Świsłocka et al. 2008, 2013).

Humans can also influence the genetic structure of small mammals—a phenomenon that has been already presented in this article with the example of common vole populations introduced to the Orkney Islands by the Neolithic people (Martínkovà et al. 2013). In Poland, however, there is no evidence that anthropogenic factors have shaped the distribution of haplogroups in bank vole, weasel, common vole, or field vole populations. Nevertheless, contemporary agriculture, cultivation of monocultures, and use of pesticides could have played a role in changes to small mammal distributions. For instance, the population of yellow-necked mice (Apodemus flavicollis) is growing rapidly throughout the country, to the point that the rodent can now be found in many different habitats, including human houses. This leads to the displacement of other species, such as voles, and ultimately a decrease in their numbers (Authors’ personal observations, not published).

The reviewed studies suggest that anthropogenic factors could play an important role in shaping genetic structure, and should thus also be considered indirect elements in suture zone formation and maintenance (Table 1).

Conclusions

In Poland, a complex network of contact zones between different phylogenetic lineages of carnivores, ungulates, and rodents is present. However, there are also species for which no genetic structure has been found in this area. For instance, the brown bear (Ursus arctos; Davison et al. 2011; Bray et al. 2013), the European badger (Meles meles; Frantz et al. 2014), and the common shrew (Sorex araneus; Raspopova et al. 2018), each have only a single mtDNA lineage in Poland. Meanwhile, the most recent phylogeographic analyses of the wild boar (Sus scrofa) in Poland identified one haplogroup E1, with variation between two subgroups, E1a and E1c (Alexandri et al. 2012; Kusza et al. 2014; Vilaça et al. 2014). However, in the case of the boar, genetic structure has changed drastically in response to both intense harvesting and population reduction because of African swine fever (ASF) outbreaks in central and eastern Europe (Podgórski et al. 2018; Podgórski and Śmietanka 2018).

We assume that all phylogeographic studies on the different mammalian carnivore, ungulate, and rodent species presented in this review have provided indirect evidence supporting the Polish suture zone hypothesis (Remington 1968; Wójcik et al. 2010). Analyses using different molecular markers (mtDNA, microsatellite DNA) have shown that central Europe is a very dynamic and diverse study area in terms of genetic variation. The mammal species included in this article each have unique evolutionary histories and routes of post-glacial re-colonization throughout central and eastern Europe. Nevertheless, further studies regarding phylogeography and genetic diversity in this region are needed, complemented by the analysis of ancient DNA extracted from fossils (Davison et al. 2011; Edwards et al. 2012; Bray et al. 2013; Lagerholm et al. 2014) and identification of genes responsible for specific adaptations (Filipi et al. 2015).

This review demonstrates that the formation and maintenance of suture zones in central Europe is a complex process, influenced by factors such as geographic barriers, climate, and environmental conditions. These elements may not be as influential when considered separately, but they create an interesting mosaic of cause and effect when viewed holistically. As a result, any hypotheses concerning European phylogeography should not be based on narrow spatial scales, small sample sizes, or the extrapolation of results from studies conducted in adjacent areas. Preventing erroneous conclusions, avoiding incomplete interpretations of large-scale patterns of genetic diversity, and uncovering the truth of European post-glacial history are challenging tasks, but crucial for applying phylogenetic patterns to conservation genetics and ultimately the protection of endangered species and disappearing habitats.

Notes

Acknowledgments

The authors thank the anonymous reviewers for their helpful comments that significantly helped improve this manuscript. We also thank A. Michalak (Cornell University) for English language editing.

Data accessibility

This article has no additional data.

Authors’ contribution

J.S. and E.T. participated in conceptualizing and writing the manuscript. Both authors approved the final version of the manuscript and agree to be held accountable for the content therein.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. 1.Mammal Research Institute Polish Academy of SciencesBiałowieżaPoland

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